An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome

John, Uwe; Lu, Yameng; Wohlrab, Sylke; Groth, Marco; Janouškovec, Jan; Kohli, Gurjeet S.; Mark, Felix Christopher; Bickmeyer, Ulf; Farhat, Sarah; Felder, Marius; Frickenhaus, Stephan; Guillou, Laure; Keeling, Patrick J.; Moustafa, Ahmed; Porcel, Betina M.; Valentin, Klaus; Glöckner, Gernot

doi:10.1126/sciadv.aav1110

Cited by 91 publications

(78 citation statements)

References 42 publications

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“…However, as mitochondria are defined based on the use of oxygen as electron acceptor (21), and usually the presence of an mt genome (but see ref. 22), we conclude that H. salminicola possesses MROs rather than true mitochondria. Although MROs have evolved several times independently, some of them present striking similarities (1,2).…”

Section: Discussionmentioning

confidence: 70%

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Yahalomi

Atkinson

Neuhof

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Although aerobic respiration is a hallmark of eukaryotes, a few unicellular lineages, growing in hypoxic environments, have secondarily lost this ability. In the absence of oxygen, the mitochondria of these organisms have lost all or parts of their genomes and evolved into mitochondria-related organelles (MROs). There has been debate regarding the presence of MROs in animals. Using deep sequencing approaches, we discovered that a member of the Cnidaria, the myxozoan Henneguya salminicola, has no mitochondrial genome, and thus has lost the ability to perform aerobic cellular respiration. This indicates that these core eukaryotic features are not ubiquitous among animals. Our analyses suggest that H. salminicola lost not only its mitochondrial genome but also nearly all nuclear genes involved in transcription and replication of the mitochondrial genome. In contrast, we identified many genes that encode proteins involved in other mitochondrial pathways and determined that genes involved in aerobic respiration or mitochondrial DNA replication were either absent or present only as pseudogenes. As a control, we used the same sequencing and annotation methods to show that a closely related myxozoan, Myxobolus squamalis, has a mitochondrial genome. The molecular results are supported by fluorescence micrographs, which show the presence of mitochondrial DNA in M. squamalis, but not in H. salminicola. Our discovery confirms that adaptation to an anaerobic environment is not unique to single-celled eukaryotes, but has also evolved in a multicellular, parasitic animal. Hence, H. salminicola provides an opportunity for understanding the evolutionary transition from an aerobic to an exclusive anaerobic metabolism.

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Section: Discussionmentioning

confidence: 70%

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Yahalomi

Atkinson

Neuhof

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…This study This study Aranda et al 13 Shoguchi et al 14 Liu et al 12 Liu et al 12 John et al 16 Gornik…”

Section: Referencementioning

confidence: 77%

“…health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e.…”

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confidence: 99%

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Stephens

González‐Pech

Cheng

et al. 2019

Preprint

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Dinoflagellates are taxonomically diverse, ecologically important phytoplankton in marine and freshwater environments. Here, we present two draft diploid genome assemblies of the free-living dinoflagellate Polarella glacialis, isolated from the Arctic and Antarctica. For each genome, guided using full-length transcriptome data, we predicted >50,000 high-quality genes. About 68% of the genome is repetitive sequence; long terminal repeats likely contribute to intra-species structural divergence and distinct genome sizes (3.0 and 2.7 Gbp).Of all genes, ~40% are encoded unidirectionally, ~25% comprised of single exons. Multigenome comparison unveiled genes specific to P. glacialis and a common, putatively bacterial, origin of ice-binding domains in cold-adapted dinoflagellates. Our results elucidate how selection acts within the context of a complex genome structure to facilitate local adaptation. Since most dinoflagellate genes are constitutively expressed, Polarella glacialis has enhanced transcriptional responses via unidirectional, tandem duplication of single-exon genes that encode functions critical to survival in cold, low-light environments. health risks 6 . Some taxa have specialised to inhabit extreme environments, such as those found in the brine channels of polar sea ice 7-10 .Thus far, available genome data of dinoflagellates are largely restricted to symbiotic or parasitic species [11][12][13][14][15][16][17] . These lineages were chosen for sequencing because their genomes are relatively small, i.e. 0.12-4.8 Gbp. In comparison, genomes of other free-living dinoflagellates are much larger in size, ranging from ~7 Gbp in the psychrophile Polarella glacialis, to over 200 Gbp in Prorocentrum sp. based on DAPI-staining of DNA content 18 .Repeat content has been estimated at >55% in the genome sequences of some free-living dinoflagellates 19,20 ; single-exon genes have also been described 21 . Given that most dinoflagellate lineages are free-living, whole genome sequences of these taxa are critical to understand the molecular mechanisms that underpin their successful diversification in specialised environmental niches.Polarella glacialis, a psychrophilic (cold-adapted) free-living species, represents an excellent system for genomic studies of dinoflagellates for three reasons. First, it is closely related to Symbiodiniaceae (both in Order Suessiales), the family that contains the coral reef symbionts, e.g. Symbiodinium and related genera. Second, P. glacialis has been reported only in polar regions. Studying the P. glacialis genome can thus provide a first glimpse into molecular mechanisms that underlie both the evolutionary transition of dinoflagellates from a free-living to a symbiotic lifestyle, and the adaptation to extreme environments. Third, the estimated genome size of P. glacialis is still in the smaller range (~7 Gbp 18 ) of all dinoflagellate taxa, which presents a technical advantage in terms of allowing efficient genome assembly and gene prediction.

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“…The identification of PKS genes in dinoflagellates has been hampered by their enormous genome sizes to obtain genome sequences, with the exception of Symbiodinium spp. [31,69,70,71] and the parasite Amoebophyya ceratii [72], which have comparatively compact genome sizes. Most studies to date have therefore been limited to transcriptome analysis, which has yielded a consensus that dinoflagellates possess both Type I modular and standalone PKS domains that may function in concert with modular PKSs by providing activity in trans, and/ or may form separate Type II -like complexes [73,74].…”

Section: Discussionmentioning

confidence: 99%

Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia

et al. 2020

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Marine dinoflagellates produce a diversity of polyketide toxins that are accumulated in marine food webs and are responsible for a variety of seafood poisonings. Reef-associated dinoflagellates of the genus Gambierdiscus produce toxins responsible for ciguatera poisoning (CP), which causes over 50,000 cases of illness annually worldwide. The biosynthetic machinery for dinoflagellate polyketides remains poorly understood. Recent transcriptomic and genomic sequencing projects have revealed the presence of Type I modular polyketide synthases in dinoflagellates, as well as a plethora of single domain transcripts with Type I sequence homology. The current transcriptome analysis compares polyketide synthase (PKS) gene transcripts expressed in two species of Gambierdiscus from French Polynesia: a highly toxic ciguatoxin producer, G. polynesiensis, versus a non-ciguatoxic species G. pacificus, each assembled from approximately 180 million Illumina 125 nt reads using Trinity, and compares their PKS content with previously published data from other Gambierdiscus species and more distantly related dinoflagellates. Both modular and single-domain PKS transcripts were present. Single domain β-ketoacyl synthase (KS) transcripts were highly amplified in both species (98 in G. polynesiensis, 99 in G. pacificus), with smaller numbers of standalone acyl transferase (AT), ketoacyl reductase (KR), dehydratase (DH), enoyl reductase (ER), and thioesterase (TE) domains. G. polynesiensis expressed both a larger number of multidomain PKSs, and larger numbers of modules per transcript, than the non-ciguatoxic G. pacificus. The largest PKS transcript in G. polynesiensis encoded a

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An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome

Cited by 91 publications

References 42 publications

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Polarella glacialis genomes encode tandem repeats of single-exon genes with functions critical to adaptation of dinoflagellates

Transcriptomic analysis of polyketide synthases in a highly ciguatoxic dinoflagellate, Gambierdiscus polynesiensis and low toxicity Gambierdiscus pacificus, from French Polynesia

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